Abstract
Filamentation temperature-sensitive H (FtsH) is an ATP-dependent zinc metalloprotease involved in diverse biological functions. There are 12 FtsH proteins in Arabidopsis, among which AtFtsH2 plays an important role in regulating the turnover of photosystem II (PSII) reaction center D1 protein and the development of the photosynthetic apparatus. Here, we have identified 11 FtsH genes in the soybean genome by a bioinformatics approach. These soybean FtsH genes corresponded to seven Arabidopsis FtsH genes, suggesting that the main characteristics of soybean FtsH genes were formed before the evolutionary split of soybean and Arabidopsis. Phylogenetic analyses allowed us to clone a soybean AtFtsH2-like gene designated as GmFtsH9. The predicted protein of GmFtsH9 consists of 690 amino acids and contains three typical FtsH proteins conserved domains. The expression level of GmFtsH9 was determined in a soybean recombinant inbred line population under a pot experiment conducted for measuring chlorophyll a fluorescence transient parameters, photosynthetic CO2 fixation rate (P N), and seed yield. Expression quantitative trait loci (eQTL) mapping revealed two trans-acting eQTLs for GmFtsH9. The significant correlation of gene expression level with chlorophyll a fluorescence transient parameters and the presence of overlapping eQTL (QTL) between gene expression level and chlorophyll a fluorescence transient parameters indicated that GmFtsH9 could be involved in regulating PSII function. These results further lead to the understanding of the mechanism underlying FtsH gene expression, and contribute to the development of marker-assisted selection breeding programs for modulating soybean FtsH gene expression.
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Abbreviations
- ABS/RC:
-
Light energy absorbed by per RC
- eQTL:
-
Expression quantitative trait locus
- ETo/TRo (ψEo):
-
Probability that a trapped exciton moves an electron into the electron transport chain beyond Q −A
- Fv/Fm:
-
Ratio of variable fluorescence to maximum fluorescence in the dark-adapted state, related to maximum quantum yield of PSII primary photochemistry
- Fv′/Fm′:
-
Ratio of variable fluorescence to maximum fluorescence in the light-adapted state, related to the maximum quantum yield of PSII primary photochemistry
- JIP-test:
-
A procedure for quantification of prompt fluorescence transients
- PIABS :
-
Performance index on absorption basis, PIABS = (RC/ABS)[φPo/(1 − φPo)][ψEo/(1 − ψEo)]
- P N :
-
Photosynthetic CO2 fixation rate
- ΦPSII:
-
Actual quantum yield of PSII primary photochemistry in the light-adapted state
- qN:
-
Non-photochemical quenching coefficient
- qP:
-
Photochemical quenching coefficient
- QTL:
-
Quantitative trait locus
- RC:
-
Reaction center of PSII
- REo/ETo (δRo):
-
Probability that an electron beyond Q −A reduces photosystem I acceptors
- RIL:
-
Recombinant inbred line
- TRo/ABS (φPo):
-
Flux ratio of trapping per absorption, φPo ≡ 1 – F 0/F M = F V/F M
References
Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141
Bilger W, Schreiber U (1986) Energy-dependent quenching of dark-level chlorophyll fluorescence in intact leaves. Photosynth Res 10:303–308
Chen J, Burke JJ, Velten J, Xin Z (2006) FtsH11 protease plays a critical role in Arabidopsis thermotolerance. Plant J 48:73–84
Doss S, Schadt EE, Drake TA, Lusis AJ (2005) Cis-acting expression quantitative trait loci in mice. Genome Res 15:681–691
Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer ELL, Eddy SR, Bateman A (2010) The pfam protein families database. Nucleic Acids Res 38:D211–D222
Fu S, Zhan Y, Zhi H, Gai J, Yu D (2006) Mapping of SMV resistance gene Rsc-7 by SSR markers in soybean. Genetica 128:63–69
Genty B, Briantais J-M, Baker N (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 900:87–92
Grant D, Cregan P, Shoemaker RC (2000) Genome organization in dicots: genome duplication in Arabidopsis and synteny between soybean and Arabidopsis. Proc Natl Acad Sci USA 97:4168–4173
Hugueney P, Bouvier F, Badillo A, d’Harlingue A, Kuntz M, Camara B (1995) Identification of a plastid protein involved in vesicle fusion and/or membrane protein translocation. Proc Natl Acad Sci USA 92:5630–5634
Ito K, Akiyama Y (2005) Cellular function, mechanism of action, and regulation of FtsH protease. Annu Rev Microbiol 59:211–231
Ivashuta S, Imai R, Uchiyama K, Gau M, Shimamoto Y (2002) Changes in chloroplast FtsH-like gene during cold acclimation in alfalfa (Medicago sativa). J Plant Physiol 159:85–90
Jansen RC, Nap JP (2001) Genetical genomics: The added value from segregation. Trends Genet 17:388–391
Kato Y, Sakamoto W (2009) Protein quality control in chloroplasts: a current model of D1 protein degradation in the photosystem II repair cycle. J Biochem 146:463–469
Kato Y, Miura E, Ido K, Ifuku K, Sakamoto W (2009) The variegated mutants lacking chloroplastic FtsHs are defective in D1 degradation and accumulate reactive oxygen species. Plant Physiol 151:1790–1801
Kolodziejczak M, Kolaczkowska A, Szczesny B, Urantowka A, Knorpp C, Kieleczawa J, Janska H (2002) A higher plant mitochondrial homologue of the yeast m-AAA protease. J Biol Chem 277:43792–43798
Lazár D (2009) Modelling of light-induced chlorophyll a fluorescence rise (O-J-I-P transient) and changes in 820 nm-transmittance signal. Photosynthetica 47:483–498
Lindahl M, Tabak S, Cseke L, Pichersky E, Andersson B, Adam Z (1996) Identification, characterization, and molecular cloning of a homologue of the bacterial FtsH protease in chloroplasts of higher plants. J Biol Chem 271:29329–29334
Liu X, Yu F, Rodermel S (2010) Arabidopsis chloroplast FtsH, var2 and suppressors of var2 leaf variegation: a review. J Integr Plant Biol 52:750–761
Mann NH, Novac N, Mullineaux CW, Newman J, Bailey S, Robinson C (2000) Involvement of an FtsH homologue in the assembly of functional photosystem II in the cyanobacterium Synechocystis sp. Pcc 6803. FEBS Lett 479:72–77
Ogura T, Wilkinson AJ (2001) AAA + superfamily ATPases: Common structure–diverse function. Genes Cells 6:575–597
Ostersetzer O, Adam Z (1997) Light-stimulated degradation of an unassembled Rieske FeS protein by a thylakoid-bound protease: the possible role of the FtsH protease. Plant Cell 9:957–965
Paillotin G (1976) Movement of excitations in the photosynthetic domains of photosystem II. J Theor Biol 58:237–252
Papageorgiou GC, Govindjee (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Kluwer, Dordrecht
Potokina E, Prasad M, Malysheva L, Röder M, Graner A (2006) Expression genetics and haplotype analysis reveal cis regulation of serine carboxypeptidase I (cxp1). A candidate gene for malting quality in barley (Hordeum vulgare l.). Funct Integr Genom 6:25–35
Santos D, De Almeida DF (1975) Isolation and characterization of a new temperature-sensitive cell division mutant of Escherichia coli K-12. J Bacteriol 124:1502–1507
Schumann W (1999) FtsH—a single-chain charonin? FEMS Microbiol Rev 23:1–11
Seo S, Okamoto M, Iwai T, Iwano M, Fukui K, Isogai A, Nakajima N, Ohashi Y (2000) Reduced levels of chloroplast FtsH protein in tobacco mosaic virus-infected tobacco leaves accelerate the hypersensitive reaction. Plant Cell 12:917–932
Shoemaker RC, Schlueter J, Doyle JJ (2006) Paleopolyploidy and gene duplication in soybean and other legumes. Curr Opin Plant Biol 9:104–109
Silva P, Thompson E, Bailey S, Kruse O, Mullineaux CW, Robinson C, Mann NH, Nixon PJ (2003) FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp PCC 6803. Plant Cell 15:2152–2164
Sinvany-Villalobo G, Davydov O, Ben-Ari G, Zaltsman A, Raskind A, Adam Z (2004) Expression in multigene families. Analysis of chloroplast and mitochondrial proteases. Plant Physiol 135:1336–1345
Stirbet A, Govindjee Z (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: Basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B (in press)
Strasser RJ, Srivastava A, Tsimilli-Michael M (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou G, Govindjee (eds) Chlorophyll fluorescence a signature of photosynthesis. Advances in photosynthesis and respiration. Springer, Dordrecht, pp 321–362
Sun A, Yi S, Yang J, Zhao C, Liu J (2006) Identification and characterization of a heat-inducible FtsH gene from tomato (Lycopersicon esculentum Mill.). Plant Sci 170:551–562
Tepperman JM, Zhu T, Chang HS, Wang X, Quail PH (2001) Multiple transcription-factor genes are early targets of phytochrome A signaling. Proc Natl Acad Sci USA 98:9437–9442
Thumma BR, Naidu BP, Chandra A, Cameron DF, Bahnisch LM, Liu C (2001) Identification of causal relationships among traits related to drought resistance in Stylosanthes scabra using QTL analysis. J Exp Bot 52:203–214
Tyystjarvi E, Aro EM (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Natl Acad Sci USA 93:2213–2218
Wang SC, Basten CJ, Zeng ZB (2005) Windows QTL Cartographer v2.5. Department of Statistics, North Carolina State University, Raleigh
Xu Y (1997) Quantitative trait loci, separating, pyramiding, and cloning. Plant Breed Rev 15:85–139
Yang Z, Wang X, Gu S, Hu Z, Xu H, Xu C (2008) Comparative study of SBP-box gene family in Arabidopsis and rice. Gene 407:1–11
Yin Z, Meng F, Song H, He X, Xu X, Yu D (2010a) Mapping quantitative trait loci associated with chlorophyll a fluorescence parameters in soybean (Glycine max (L.) Merr.). Planta 231:875–885
Yin Z, Meng F, Song H, Wang X, Xu X, Yu D (2010b) Expression quantitative trait loci analysis of two genes encoding Rubisco activase in soybean. Plant Physiol 152:1625–1637
Yoshioka M, Uchida S, Mori H, Komayama K, Ohira S, Morita N, Nakanishi T, Yamamoto Y (2006) Quality control of photosystem II. J Biol Chem 281:21660–21669
Yu F, Park S, Rodermel SR (2004) The Arabidopsis FtsH metalloprotease gene family: interchangeability of subunits in chloroplast oligomeric complexes. Plant J 37:864–876
Yu F, Park S, Rodermel SR (2005) Functional redundancy of AtFtsH metalloproteases in thylakoid membrane complexes. Plant Physiol 138:1957–1966
Yue G, Hu X, He Y, Yang A, Zhang J (2010) Identification and characterization of two members of two members of the FtsH gene family in maize (Zea mays L.). Mol Biol Rep 37:855–863
Zaltsman A, Ori N, Adam Z (2005) Two types of FtsH protease subunits are required for chloroplast biogenesis and photosystem II repair in Arabidopsis. Plant Cell 17:2782–2790
Zelisko A, Garcia-Lorenzo M, Jackowski G, Jansson S, Funk C (2005) AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence. Proc Natl Acad Sci USA 102:13699–13704
Zhang XC, Wu X, Findley S, Wan J, Libault M, Nguyen HT, Cannon SB, Stacey G (2007) Molecular evolution of lysin motif-type receptor-like kinases in plants. Plant Physiol 144:623–636
Zhang D, Kato Y, Zhang L, Fujimoto M, Tsutsumi N, Sodmergen SakamotoW (2010) The FtsH protease heterocomplex in Arabidopsis: dispensability of type-B protease activity for proper chloroplast development. Plant Cell 22:3710–3725
Acknowledgments
This work was supported in part by the National Key Basic Research Program of China (973 Program) (2010CB125906, 2009CB118400), the National Natural Science Foundation of China (31000718, 30800692). We thank Dr. Han Zhao from the Jiangsu Academy of Agricultural Science for assistance in bioinformatics analysis of soybean FtsH genes, and the two anonymous reviewers for their valuable comments and discussions.
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Z. Yin and F. Meng contributed equally to this work.
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Yin, Z., Meng, F., Song, H. et al. GmFtsH9 expression correlates with in vivo photosystem II function: chlorophyll a fluorescence transient analysis and eQTL mapping in soybean. Planta 234, 815–827 (2011). https://doi.org/10.1007/s00425-011-1445-5
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DOI: https://doi.org/10.1007/s00425-011-1445-5